Inflammatory doses of UV may not be necessary for skin carcinogenesis

Photochemistry and Photobiology

Volumn 84, Issue 2, 2008, Pages 272-283

  Halliday, Gary M ^a   Lyons, J Guy ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b ROYAL PRINCE ALFRED HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; HUMAN; MOUSE; RADIATION INJURY; RADIATION RESPONSE; REVIEW; SKIN TUMOR; ULTRAVIOLET RADIATION;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, RADIATION; HUMANS; MICE; NEOPLASMS, RADIATION-INDUCED; SKIN NEOPLASMS; ULTRAVIOLET RAYS;

EID: 41049106406     PISSN: 00318655     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1751-1097.2007.00247.x     Document Type: Review

References (152)

1. Mukhtar, H., P. D. Forbes H. N. Ananthaswamy (1999) Photocarcinogenesis - Models and mechanisms. Photodermatol. Photoimmunol. Photomed. 15, 91 95.
2. Afaq, F., N. Ahmad H. Mukhtar (2003) Suppression of UVB-induced phosphorylation of mitogen-activated protein kinases and nuclear factor kappa B by green tea polyphenol in SKH-1 hairless mice. Oncogene 22, 9254 9264.
3. Afaq, F., M. Saleem, C. G. Krueger, J. D. Reed H. Mukhtar (2005) Anthocyanin- and hydrolyzable tannin-rich pomegranate fruit extract modulates MAPK and NF-kappa B pathways and inhibits skin tumorigenesis in CD-1 mice. Int. J. Cancer 113, 423 433.
4. Afaq, F., V. M. Adhami H. Mukhtar (2005) Photochemoprevention of ultraviolet B signaling and photocarcinogenesis. Mutat. Res. 571, 153 173.
5. Syed, D. N., A. Malik, N. Hadi, S. Sarfaraz, F. Afaq H. Mukhtar (2006) Photochemopreventive effect of pomegranate fruit extract on UVA-mediated activation of cellular pathways in normal human epidermal keratinocytes. Photochem. Photobiol. 82, 398 405.
6. Fisher, M. S. M. L. Kripke (1982) Suppressor T lymphocytes control the development of primary skin cancers in ultraviolet-irradiated mice. Science 216, 1133 1134.
7. Donawho, C. K. M. L. Kripke (1991) Evidence that the local effect of ultraviolet radiation on the growth of murine melanomas is immunologically mediated. Cancer Res. 51, 4176 4181.
8. Cavanagh, L. L. G. M. Halliday (1996) Dendritic epidermal T cells in ultraviolet-irradiated skin enhance skin tumor growth by inhibiting CD4(+) T-cell-mediated immunity. Cancer Res. 56, 2607 2615.
9. Sluyter, R. G. M. Halliday (2000) Enhanced tumor growth in UV-irradiated skin is associated with an influx of inflammatory cells into the epidermis. Carcinogenesis 21, 1801 1807.
10. Halliday, G. M., A. Patel, M. J. Hunt, F. J. Tefany R. S. C. Barnetson (1995) Spontaneous regression of human melanoma/non-melanoma skin cancer: Association with infiltrating CD4+ T cells. World J Surg. 19, 352 358.
11. Lowes, M. A., G. A. Bishop, K. Crotty, R. S. Barnetson G. M. Halliday (1997) T helper 1 cytokine MRNA is increased in spontaneously regressing primary melanomas. J. Invest. Dermatol. 108, 914 919.
12. Menzies, S. W. W. H. McCarthy (1997) Complete regression of primary cutaneous malignant melanoma. Arch. Surg. 132, 553 556.
13. Cerottini, J. C., D. Lienard P. Romero (1996) Recognition of tumor-associated antigens by T-lymphocytes - Perspectives for peptide-based vaccines. Ann. Oncol. 7, 339 342.
14. Yarosh, D. B., A. V. Pena, S. L. Nay, M. T. Canning D. A. Brown (2005) Calcineurin inhibitors decrease DNA repair and apoptosis in human keratinocytes following ultraviolet B irradiation. J. Invest. Dermatol. 125, 1020 1025.
15. Patel, A. S., M. R. Karagas, A. E. Perry, S. K. Spencer H. H. Nelson (2007) Gene-drug interaction at the glucocorticoid receptor increases risk of squamous cell skin cancer. J. Invest. Dermatol. 127, 1868 1870.
16. Moloney, F., P. Kelly, E. Kay, P. Conlon G. Murphy (2004) Maintenance versus reduction of immunosuppression in renal transplant recipients with aggressive squamous cell carcinoma. Dermatol. Surg. 30, 674 678.
17. Cohen, S. M. L. B. Ellwein (1991) Genetic errors, cell proliferation, and carcinogenesis. Cancer Res. 51, 6493 6505.
18. Kangsamaksin, T., H. J. Park, C. S. Trempus R. J. Morris (2007) A perspective on murine keratinocyte stem cells as targets of chemically induced skin cancer. Mol. Carcinog. 46, 579 584.
19. Ananthaswamy, H. N. S. Kanjilal (1996) Oncogenes and tumor suppressor genes in photocarcinogenesis. Photochem. Photobiol. 63, 428 432.
20. Ananthaswamy, H. N., A. Fourtanier, R. L. Evans, S. Tison, C. Medaisko, S. E. Ullrich M. L. Kripke (1998) p53 Mutations in hairless SKH-hr1 mouse skin tumors induced by a solar simulator. Photochem. Photobiol. 67, 227 232.
21. Rebel, H., N. Kram, A. Westerman, S. Banus, H. J. van Kranen F. R. de Gruijl (2005) Relationship between UV-induced mutant p53 patches and skin tumours, analysed by mutation spectra and by induction kinetics in various DNA-repair-deficient mice. Carcinogenesis 26, 2123 2130.
22. Adolphe, C., R. Hetherington, T. Ellis B. Wainwright (2006) Patched1 functions as a gatekeeper by promoting cell cycle progression. Cancer Res. 66, 2081 2088.
23. Gray-Schopfer, V., C. Wellbrock R. Marais (2007) Melanoma biology and new targeted therapy. Nature 445, 851 857.
24. Sluyter, R. G. M. Halliday (2001) Infiltration by inflammatory cells required for solar-simulated ultraviolet radiation enhancement of skin tumor growth. Cancer Immunol. Immunother. 50, 151 156.
25. Ying, C. Y., J. A. Parrish M. A. Pathak (1974) Additive erythemogenic effects of middle-(280-320 nm) and long-(320-400 nm) wave ultraviolet light. J. Invest. Dermatol. 63, 273 278.
26. Young, A. R., C. A. Chadwick, G. I. Harrison, O. Nikaido, J. Ramsden C. S. Potten (1998) The similarity of action spectra for thymine dimers in human epidermis and erythema suggests that DNA is the chromophore for erythema. J. Invest. Dermatol. 111, 982 988.
27. McKinlay, A. F. B. L. Diffey (1987) A reference action spectrum for ultraviolet induced erythema in human skin. CIE J. 6, 17 22.
28. Berg, R. J., A. de Vries, H. van Steeg F. R. de Gruijl (1997) Relative susceptibilities of XPA knockout mice and their heterozygous and wild-type littermates to UVB-induced skin cancer. Cancer Res. 57, 581 584.
29. Berg, R. J., H. Rebel, G. T. van der Horst, H. J. van Kranen, L. H. Mullenders, W. A. van Vloten F. R. de Gruijl (2000) Impact of global genome repair versus transcription-coupled repair on ultraviolet carcinogenesis in hairless mice. Cancer Res. 60, 2858 2863.
30. Ley, R. D. (1997) Ultraviolet radiation A-induced precursors of cutaneous melanoma in Monodelphis domestica. Cancer Res. 57, 3682 3684.
31. Melnikova, V. O., A. Pacifico, S. Chimenti, K. Peris H. N. Ananthaswamy (2005) Fate of UVB-induced p53 mutations in SKH-hr1 mouse skin after discontinuation of irradiation: Relationship to skin cancer development. Oncogene 24, 7055 7063.
32. Russo, P. A. J. G. M. Halliday (2006) Inhibition of nitric oxide and reactive oxygen species production improves the ability of a sunscreen to protect from sunburn, immunosuppression and photocarcinogenesis. Br. J. Dermatol. 155, 408 415.
33. Ananthaswamy, H. N., S. E. Ullrich, R. E. Mascotto, A. Fourtanier, S. M. Loughlin, P. Khaskina, C. D. Bucana M. L. Kripke (1999) Inhibition of solar simulator-induced p53 mutations and protection against skin cancer development in mice by sunscreens. J. Invest. Dermatol. 112, 763 768.
34. Matsumura, Y., A. M. Moodycliffe, D. X. Nghiem, S. E. Ullrich H. N. Ananthaswamy (2004) Resistance of CD1d-/- mice to ultraviolet-induced skin cancer is associated with increased apoptosis. Am. J. Pathol. 165, 879 887.
35. De Gruijl, F. R., H. J. C. M. Sterenborg, P. D. Forbes, R. E. Davies, C. Cole, G. Kelfkens, H. Vanweelden, H. Slaper J. C. van der Leun (1993) Wavelength dependence of skin cancer induction by ultraviolet irradiation of albino hairless mice. Cancer Res. 53, 53 60.
36. Sterenborg, H. J. C. M. J. C. van der Leun (1990) Tumorigenesis by a long wavelength UV-A source. Photochem. Photobiol. 51, 325 330.
37. Kelfkens, G., F. R. de Gruijl J. C. van der Leun (1991) Tumorigenesis by short-wave ultraviolet A: Papillomas versus squamous cell carcinomas. Carcinogenesis 12, 1377 1382.
38. Berg, R. J. W., F. R. De Gruijl J. C. van der Leun (1993) Interaction between ultraviolet-A and ultraviolet-B radiations in skin cancer induction in hairless mice. Cancer Res. 53, 4212 4217.
39. Friedmann, A. C., G. M. Halliday, R. S. Barnetson, V. E. Reeve, C. Walker, C. R. S. Patterson D. L. Damian (2004) The topical isoflavonoid NV-07 alpha reduces solar-simulated UV-induced suppression of Mantoux reactions in humans. Photochem. Photobiol. 80, 416 421.
40. Strickland, P. T. (1986) Photocarcinogenesis by near-ultraviolet (UVA) radiation in Sencar mice. J. Invest. Dermatol. 87, 272 275.
41. Berking, C., R. Takemoto, R. L. Binder, S. M. Hartman, D. J. Ruiter, P. M. Gallagher, S. R. Lessin M. Herlyn (2002) Photocarcinogenesis in human adult skin grafts. Carcinogenesis 23, 181 187.
42. Klein-Szanto, A. J. P., W. K. Silvers B. Mintz (1994) Ultraviolet radiation-induced malignant skin melanoma in melanoma-susceptible transgenic mice. Cancer Res. 54, 4569 4572.
43. Setlow, R. B., E. Grist, K. Thompson A. D. Woodhead (1993) Wavelengths effective in induction of malignant melanoma. Proc. Natl Acad. Sci. USA 90, 6666 6670.
44. Noonan, F. P., J. A. Recio, H. Takayama, P. Duray, M. R. Anver, W. L. Rush, E. C. De Fabo G. Merlino (2001) Neonatal sunburn and melanoma in mice. Nature 413, 271 272.
45. Recio, J. A., F. P. Noonan, H. Takayama, M. R. Anver, P. Duray, W. L. Rush, G. Lindner, E. C. De Fabo, R. A. DePinho G. Merlino (2002) Ink4a/Arf deficiency promotes ultraviolet radiation-induced melanomagenesis. Cancer Res. 62, 6724 6730.
46. Atillasoy, E. S., J. T. Seykora, P. W. Soballe, R. Elenitsas, M. Nesbit, D. E. Elder, K. T. Montone, E. Sauter M. Herlyn (1998) UVB induces atypical melanocytic lesions and melanoma in human skin. Am. J. Pathol. 152, 1179 1186.
47. Yoshikawa, T., V. Rae, W. Bruins-Slot, J. W. Van den Berg, J. R. Taylor J. W. Streilein (1990) Susceptibility to effects of UVB radiation on induction of contact hypersensitivity as a risk factor for skin cancer in humans. J. Invest. Dermatol. 95, 530 536.
48. Cooper, K. D., L. Oberhelman, T. A. Hamilton, O. Baadsgaard, M. Terhune, G. Levee, T. Anderson H. Koren (1992) UV exposure reduces immunization rates and promotes tolerance to epicutaneous antigens in humans - Relationship to dose, CD1a-DR+ epidermal macrophage induction, and Langerhans cell depletion. Proc. Natl Acad. Sci. USA 89, 8497 8501.
49. Damian, D. L., R. S. Barnetson G. M. Halliday (1999) Low-dose UVA and UVB have different time courses for suppression of contact hypersensitivity to a recall antigen in humans. J. Invest. Dermatol. 112, 939 944.
50. Poon, T. S. C., R. S. C. Barnetson G. M. Halliday (2005) Sunlight-induced immunosuppression in humans is initially because of UVB, then UVA, followed by interactive effects. J. Invest. Dermatol. 125, 840 846.
51. Byrne, S. N., N. Spinks G. M. Halliday (2002) Ultraviolet A irradiation of C57BL/6 mice suppresses systemic contact hypersensitivity or enhances secondary immunity depending on dose. J. Invest. Dermatol. 119, 858 864.
52. Bestak, R. G. M. Halliday (1996) Chronic low-dose UVA irradiation induces local suppression of contact hypersensitivity, Langerhans cell depletion and suppressor cell activation in C3H/HeJ mice. Photochem. Photobiol. 64, 969 974.
53. Nghiem, D. X., N. Kazimi, G. Clydesdale, H. N. Ananthaswamy, M. L. Kripke S. E. Ullrich (2001) Ultraviolet A radiation suppresses an established immune response: Implications for sunscreen design. J. Invest. Dermatol. 117, 1193 1199.
54. Fourtanier, A., D. Moyal, J. Maccario, D. Compan, P. Wolf, F. Quehenberger, K. Cooper, E. Baron, G. Halliday, T. Poon, P. Seed, S. L. Walker A. R. Young (2005) Measurement of sunscreen immune protection factors in humans: A consensus paper. J. Invest. Dermatol. 125, 403 409.
55. Moyal, D. D. A. M. Fourtanier (2001) Broad-spectrum sunscreens provide better protection from the suppression of the elicitation phase of delayed-type hypersensitivity response in humans. J. Invest. Dermatol. 117, 1186 1192.
56. Hersey, P., M. Bradley, E. Hasic, G. Haran, A. Edwards W. H. McCarthy (1983) Immunological effects of solarium exposure. Lancet 321, 545 548.
57. Kelly, D. A., A. R. Young, J. M. McGregor, P. T. Seed, C. S. Potten S. L. Walker (2000) Sensitivity to sunburn is associated with susceptibility to ultraviolet radiation-induced suppression of cutaneous cell-mediated immunity. J. Exp. Med. 191, 561 566.
58. Warren, J. B., R. K. Loi M. L. Coughlan (1993) Involvement of nitric oxide synthase in the delayed vasodilator response to ultraviolet light irradiation of rat skin in vivo. Br. J. Pharmacol. 109, 802 806.
59. Weller, R. (1997) Nitric oxide - A newly discovered chemical transmitter in human skin. Br. J. Dermatol. 137, 665 672.
60. Hruza, L. L. A. P. Pentland (1993) Mechanisms of UV-induced inflammation. J. Invest. Dermatol. 100, S35 S41.
61. Setlow, R. B. (2002) Shedding light on proteins, nucleic acids, cells, humans and fish. Mutat. Res. 511, 1 14.
62. Brash, D. E., J. A. Rudolph, J. A. Simon, A. Lin, G. J. Mckenna, H. P. Baden, A. J. Halperin J. Ponten (1991) A role for sunlight in skin cancer-UV-induced p53 mutations in squamous cell carcinoma. Proc. Natl Acad. Sci. USA 88, 10124 10128.
63. Robert, C., B. Muel, A. Benoit, L. Dubertret, A. Sarasin A. Stary (1996) Cell survival and shuttle vector mutagenesis induced by ultraviolet A and ultraviolet B radiation in a human cell line. J. Invest. Dermatol. 106, 721 728.
64. Drobetsky, E. A., J. Turcotte A. Chateauneuf (1995) A role for ultraviolet A in solar mutagenesis. Proc. Natl Acad. Sci. USA 92, 2350 2354.
65. Kawanishi, S., Y. Hiraku S. Oikawa (2001) Mechanism of guanine-specific DNA damage by oxidative stress and its role in carcinogenesis and aging. Mutat. Res. 488, 65 76.
66. Kamiya, H. (2003) Mutagenic potentials of damaged nucleic acids produced by reactive oxygen/nitrogen species: Approaches using synthetic oligonucleotides and nucleotides: Survey and summary. Nucleic Acids Res. 31, 517 531.
67. Agar, N. S., G. M. Halliday, R. S. Barnetson, H. N. Ananthaswamy, M. Wheeler A. M. Jones (2004) The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: A role for UVA in human skin carcinogenesis. Proc. Natl Acad. Sci. USA 101, 4954 4959.
68. Halliday, G. M., N. S. Agar, R. S. C. Barnetson, H. N. Ananthaswamy A. M. Jones (2005) UV-A fingerprint mutations in human skin cancer. Photochem. Photobiol. 81, 3 8.
69. Mouret, S., C. Baudouin, M. Charveron, A. Favier, J. Cadet T. Douki (2006) Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc. Natl Acad. Sci. USA 103, 13765 13770.
70. Pierceall, W. E., M. L. Kripke H. N. Ananthaswamy (1992) N-ras mutation in ultraviolet radiation-induced murine skin cancers. Cancer Res. 52, 3946 3951.
71. Kim, S. I., G. P. Pfeifer A. Besaratinia (2007) Mutagenicity of ultraviolet A radiation in the lacI transgene in Big Blue mouse embryonic fibroblasts. Mutat. Res. Fund Mol. Mech. Mutagen. 617, 71 78.
72. Besaratinia, A., S. Kim, S. E. Bates G. P. Pfeifer (2007) Riboflavin activated by ultraviolet A1 irradiation induces oxidative DNA damage-mediated mutations inhibited by vitamin C. Proc. Natl Acad. Sci. USA 104, 5953 5958.
73. Kappes, U. P., D. Luo, M. Potter, K. Schulmeister T. M. Runger (2006) Short- and long-wave UV light (UVB and UVA) induce similar mutations in human skin cells. J. Invest. Dermatol. 126, 667 675.
74. Persson, A., D. Edstrom, H. Backvall, J. Lunderberg, F. Ponten, A.-M. Ros C. Williams (2002) The mutagenic effect of ultraviolet-A1 on human skin demonstrated by sequencing the p53 gene in single keratinocytes. Photodermatol. Photoimmunol. Photomed. 18, 287 293.
75. Coussens, L. M. Z. Werb (2002) Inflammation and cancer. Nature 420, 860 867.
76. de Visser, K. E., A. Eichten L. M. Coussens (2006) Paradoxical roles of the immune system during cancer development. Nat. Rev. Cancer 6, 24 37.
77. Balkwill, F. A. Mantovani (2001) Inflammation and cancer: Back to Virchow? Lancet 357, 539 545.
78. Halliday, G. M. (2005) Inflammation, gene mutation and photoimmunosuppression in response to UVR-induced oxidative damage contributes to photocarcinogenesis. Mutat. Res. 571, 107 120.
79. Halliday, G. M. S. Le (2001) Transforming growth factor-beta produced by progressor tumors inhibits, while IL-10 produced by regressor tumors enhances, Langerhans cell migration from skin. Int. Immunol. 13, 1147 1154.
80. Weber, F., S. N. Byrne, S. Le, D. A. Brown, S. N. Breit, R. A. Scolyer G. M. Halliday (2005) Transforming growth factor-beta1 immobilises dendritic cells within skin tumours and facilitates tumour escape from the immune system. Cancer Immunol. Immunother. 54, 898 906.
81. Morelli, J. G. D. A. Norris (1993) Influence of inflammatory mediators and cytokines on human melanocyte function. J. Invest. Dermatol. 100, S191 S195.
82. Berhane, T., G. M. Halliday, B. Cooke R. S. Barnetson (2002) Inflammation is associated with progression of actinic keratoses to squamous cell carcinomas in humans. Br. J. Dermatol. 146, 810 815.
83. Thomas-Ahner, J. M., B. C. Wulff, K. L. Tober, D. F. Kusewitt, J. A. Riggenbach T. M. Oberyszyn (2007) Gender differences in UVB-induced skin carcinogenesis, inflammation, and DNA damage. Cancer Res. 67, 3468 3474.
84. Damian, D. L., C. R. S. Patterson, M. Stapelberg, J. Park, R. S. C. Barnetson G. M. Halliday (2007) Ultraviolet radiation-induced immunosuppression is greater in men and prevented by topical nicotinamide. J. Invest. Dermatol. (in press).
85. Chung, J. H. J. I. Youn (1995) Effect of ultraviolet A on IL-1 production by ultraviolet B in cultured human keratinocytes. J. Dermatol. Sci. 9, 87 93.
86. Kupper, T. S., A. O. Chua, P. Flood, J. McGuire U. Gubler (1987) Interleukin 1 gene expression in cultured human keratinocytes is augmented by ultraviolet irradiation. J. Clin. Invest. 80, 430 436.
87. r 95,000 type IV collagenase/gelatinase and interstitial fibroblast-type collagenase by rat mucosal keratinocytes. J. Biol. Chem. 268, 19143 19151.
88. Leverkus, M., M. Yaar, M. S. Eller, E. H. Tang B. A. Gilchrest (1998) Post-transcriptional regulation of UV induced TNF-alpha expression. J. Invest. Dermatol. 110, 353 357.
89. Skiba, B., B. Neill T. J. Piva (2005) Gene expression profiles of TNF-alpha, TACE, furin, IL-1beta and matrilysin in UVA- and UVB-irradiated HaCat cells. Photodermatol. Photoimmunol. Photomed. 21, 173 182.
90. Venner, T. J., D. N. Sauder, C. Feliciani R. C. McKenzie (1995) Interleukin-8 and melanoma growth-stimulating activity (GRO) are induced by ultraviolet B radiation in human keratinocyte cell lines. Exp. Dermatol. 4, 138 145.
91. Singh, R. K., M. Gutman, R. Reich M. Bar-Eli (1995) Ultraviolet B irradiation promotes tumorigenic and metastatic properties in primary cutaneous melanoma via induction of interleukin 8. Cancer Res. 55, 3669 3674.
92. Cataisson, C., A. J. Pearson, M. Z. Tsien, F. Mascia, J. L. Gao, S. Pastore S. H. Yuspa (2006) CXCR2 ligands and G-CSF mediate PKCalpha-induced intraepidermal inflammation. J. Clin. Invest. 116, 2757 2766.
93. Shimizu, T., R. Abe, A. Ohkawara J. Nishihira (1999) Ultraviolet B radiation upregulates the production of macrophage migration inhibitory factor (MIF) in human epidermal keratinocytes. J. Invest. Dermatol. 112, 210 215.
94. Hudson, J. D., M. A. Shoaibi, R. Maestro, A. Carnero, G. J. Hannon D. H. Beach (1999) A proinflammatory cytokine inhibits p53 tumor suppressor activity. J. Exp. Med. 190, 1375 1382.
95. Mitchell, R. A., H. Liao, J. Chesney, G. Fingerle-Rowson, J. Baugh, J. David R. Bucala (2002) Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: Regulatory role in the innate immune response. Proc. Natl Acad. Sci. USA 99, 345 350.
96. Petrenko, O. U. M. Moll (2005) Macrophage migration inhibitory factor MIF interferes with the Rb-E2F pathway. Mol. Cell 17, 225 236.
97. Hernandez-Pigeon, H., C. Jean, A. Charruyer, M. J. Haure, C. Baudouin, M. Charveron, A. Quillet-Mary G. Laurent (2007) UVA induces granzyme B in human keratinocytes through MIF: Implication in extracellular matrix remodeling. J. Biol. Chem. 282, 8157 8164.
98. Lyons, J. G., B. Birkedal-Hansen, W. G. I. Moore, R. L. O'Grady H. Birkedal-Hansen (1991) Characteristics of a 95 kDa matrix metalloproteinase produced by mammary carcinoma cells. Biochemistry 30, 1449 1456.
99. Van den Steen, P. E., P. Proost, A. Wuyts, J. Van Damme G. Opdenakker (2000) Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact. Blood 96, 2673 2681.
100. Steinbrenner, H., M. C. Ramos, D. Stuhlmann, H. Sies P. Brenneisen (2003) UVA-mediated downregulation of MMP-2 and MMP-9 in human epidermal keratinocytes. Biochem. Biophys. Res. Commun. 308, 486 491.
101. He, Y. Y., J. Pi, J. L. Huang, B. A. Diwan, M. P. Waalkes C. F. Chignell (2006) Chronic UVA irradiation of human HaCaT keratinocytes induces malignant transformation associated with acquired apoptotic resistance. Oncogene 25, 3680 3688.
102. Fisher, G. J., S. C. Datta, H. S. Talwar, Z.-Q. Wang, J. Varani, S. Kang J. J. Voorhees (1996) Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature 379, 335 339.
103. Min, D., A. G. Moore, M. A. Bain, S. N. Breit J. G. Lyons (2002) Activation of macrophage promatrix metalloproteinase-9 by lipopolysaccharide- associated proteinases. J. Immunol. 168, 2449 2455.
104. Bachelor, M. A. G. T. Bowden (2004) UVA-mediated activation of signaling pathways involved in skin tumor promotion and progression. Semin. Cancer Biol. 14, 131 138.
105. Bowden, G. T. (2004) Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling. Nat. Rev. Cancer 4, 23 35.
106. Khalil, Z., S. L. Townley, M. A. Grimbaldeston, J. J. Finlay-Jones P. H. Hart (2001) cis-Urocanic acid stimulates neuropeptide release from peripheral sensory nerves. J. Invest. Dermatol. 117, 886 891.
107. Rosette, C. M. Karin (1996) Ultraviolet light and osmotic stress: Activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274, 1194 1197.
108. Peus, D., R. A. Vasa, A. Beyerle, A. Meves, C. Krautmacher M. R. Pittelkow (1999) UVB activates ERK1/2 and p38 signaling pathways via reactive oxygen species in cultured keratinocytes. J. Invest. Dermatol. 112, 751 756.
109. Gonzales, M. G. T. Bowden (2002) Ultraviolet B (UVB) induction of the c-fos promoter is mediated by phospho-cAMP response element binding protein (CREB) binding to CRE and c-fos activator protein 1 site (FAP1) cis elements. Gene 293, 169 179.
110. Gonzales, M. G. T. Bowden (2002) The role of PI 3-kinase in the UVB-induced expression of c-fos. Oncogene 21, 2721 2728.
111. Chen, W. G. T. Bowden (1999) Activation of p38 MAP kinase and ERK are required for ultraviolet-B induced c-fos gene expression in human keratinocytes. Oncogene 18, 7469 7476.
112. Fritsche, E., C. Schafer, C. Calles, T. Bernsmann, T. Bernshausen, M. Wurm, U. Hubenthal, J. E. Cline, H. Hajimiragha, P. Schroeder, L. O. Klotz, A. Rannug, P. Furst, H. Hanenberg, J. Abel J. Krutmann (2007) Lightening up the UV response by identification of the arylhydrocarbon receptor as a cytoplasmatic target for ultraviolet B radiation. Proc. Natl Acad. Sci. USA 104, 8851 8856.
113. Chen, W., Q. Tang, M. S. Gonzales G. T. Bowden (2001) Role of p38 MAP kinases and ERK in mediating ultraviolet-B induced cyclooxygenase-2 gene expression in human keratinocytes. Oncogene 20, 3921 3926.
114. Tang, Q., M. Gonzales, H. Inoue G. T. Bowden (2001) Roles of Akt and glycogen synthase kinase 3beta in the ultraviolet B induction of cyclooxygenase-2 transcription in human keratinocytes. Cancer Res. 61, 4329 4332.
115. Karin, M. (2006) Nuclear factor-kappaB in cancer development and progression. Nature 441, 431 436.
116. Thyss, R., V. Virolle, V. Imbert, J. F. Peyron, D. Aberdam T. Virolle (2005) NF-kappaB/Egr-1/Gadd45 are sequentially activated upon UVB irradiation to mediate epidermal cell death. EMBO J. 24, 128 137.
117. Lewis, D. A. D. F. Spandau (2007) UVB activation of NF-kappaB in normal human keratinocytes occurs via a unique mechanism. Arch. Dermatol. Res. 299, 93 101.
118. van Hogerlinden, M., B. L. Rozell, L. Ahrlund-Richter R. Toftgard (1999) Squamous cell carcinomas and increased apoptosis in skin with inhibited Rel/nuclear factor-kappaB signaling. Cancer Res. 59, 3299 3303.
119. Setlow, R. B. (1974) The wavelengths in sunlight effective in producing skin cancer: A theoretical analysis. Proc. Natl Acad. Sci. USA 71, 3363 3366.
120. Klotz, L. O., C. Pellieux, K. Briviba, C. Pierlot, J. M. Aubry H. Sies (1999) Mitogen-activated protein kinase (p38-, JNK-, ERK-) activation pattern induced by extracellular and intracellular singlet oxygen and UVA. Eur. J. Biochem. 260, 917 922.
121. Silvers, A. L., M. A. Bachelor G. T. Bowden (2003) The role of JNK and p38 MAPK activities in UVA-induced signaling pathways leading to AP-1 activation and c-Fos expression. Neoplasia 5, 319 329.
122. Reelfs, O., R. M. Tyrrell C. Pourzand (2004) Ultraviolet A radiation-induced immediate iron release is a key modulator of the activation of NF-kappaB in human skin fibroblasts. J. Invest. Dermatol. 122, 1440 1447.
123. Vile, G. F. R. M. Tyrrell (1995) UVA radiation-induced oxidative damage to lipids and proteins in vitro and in human skin fibroblasts is dependent on iron and singlet oxygen. Free Radic. Biol. Med. 18, 721 730.
124. Silvers, A. L., J. S. Finch G. T. Bowden (2006) Inhibition of UVA-induced c-Jun N-terminal kinase activity results in caspase-dependent apoptosis in human keratinocytes. Photochem. Photobiol. 82, 423 431.
125. Katiyar, S. K., F. Afaq, A. Perez H. Mukhtar (2001) Green tea polyphenol (-)-epigallocatechin-3-gallate treatment of human skin inhibits ultraviolet radiation-induced oxidative stress. Carcinogenesis 22, 287 294.
126. Katiyar, S. K. H. Mukhtar (2001) Green tea polyphenol (-)-epigallocatechin-3-gallate treatment to mouse skin prevents UVB-induced infiltration of leukocytes, depletion of antigen-presenting cells, and oxidative stress. J. Leukoc. Biol. 69, 719 726.
127. Wang, Z. Y., R. Agarwal, D. R. Bickers H. Mukhtar (1991) Protection against ultraviolet B radiation-induced photocarcinogenesis in hairless mice by green tea polyphenols. Carcinogenesis 12, 1527 1530.
128. Ulrich, C., M. Hackethal, M. Ulrich, A. Howorka, T. Forschner, W. Sterry E. Stockfleth (2007) Treatment of multiple actinic keratoses with topical diclofenac 3% gel in organ transplant recipients: A series of six cases. Br. J. Dermatol. 156 (Suppl. 3 40 42.
129. Patel, M. J. E. Stockfleth (2007) Does progression from actinic keratosis and Bowen's disease end with treatment: Diclofenac 3% gel, an old drug in a new environment? Br. J. Dermatol. 156, 53 56.
130. Kim, K. H., E. J. Park, Y. J. Seo, H. S. Cho, C. W. Kim, K. J. Kim H. R. Park (2006) Immunohistochemical study of cyclooxygenase-2 and p53 expression in skin tumors. J. Dermatol. 33, 319 325.
131. Lejeune, F. J., Y. Monnier C. Ruegg (2006) Complete and long-lasting regression of disseminated multiple skin melanoma metastases under treatment with cyclooxygenase-2 inhibitor. Melanoma Res. 16, 263 265.
132. Fecker, L. F., E. Stockfleth, I. Nindl, C. Ulrich, T. Forschner J. Eberle (2007) The role of apoptosis in therapy and prophylaxis of epithelial tumours by nonsteroidal anti-inflammatory drugs (NSAIDs). Br. J. Dermatol. 156 (Suppl. 3 25 33.
133. An, K. P., M. Athar, X. Tang, S. K. Katiyar, J. Russo, J. Beech, M. Aszterbaum, L. Kopelovich, E. H. Epstein Jr., H. Mukhtar D. R. Bickers (2002) Cyclooxygenase-2 expression in murine and human nonmelanoma skin cancers: Implications for therapeutic approaches. Photochem. Photobiol. 76, 73 80.
134. Butler, G. J., R. Neale, A. C. Green, N. Pandeya D. C. Whiteman (2005) Nonsteroidal anti-inflammatory drugs and the risk of actinic keratoses and squamous cell cancers of the skin. J. Am. Acad. Dermatol. 53, 966 972.
135. Vogel, U., J. Christensen, H. Wallin, S. Friis, B. A. Nexo A. Tjonneland (2007) Polymorphisms in COX-2, NSAID use and risk of basal cell carcinoma in a prospective study of Danes. Mutat. Res. 617, 138 146.
136. Fischer, S. M., H. H. Lo, G. B. Gordon, K. Seibert, G. Kelloff, R. A. Lubet C. J. Conti (1999) Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, and indomethacin against ultraviolet light-induced skin carcinogenesis. Mol. Carcinog. 25, 231 240.
137. Wilgus, T. A., A. T. Koki, B. S. Zweifel, D. F. Kusewitt, P. A. Rubal T. M. Oberyszyn (2003) Inhibition of cutaneous ultraviolet light B-mediated inflammation and tumor formation with topical celecoxib treatment. Mol. Carcinog. 38, 49 58.
138. Fischer, S. M., C. J. Conti, J. Viner, C. M. Aldaz R. A. Lubet (2003) Celecoxib and difluoromethylornithine in combination have strong therapeutic activity against UV-induced skin tumors in mice. Carcinogenesis 24, 945 952.
139. Athar, M., K. P. An, X. Tang, K. D. Morel, A. L. Kim, L. Kopelovich D. R. Bickers (2004) Photoprotective effects of sulindac against ultraviolet B-induced phototoxicity in the skin of SKH-1 hairless mice. Toxicol. Appl. Pharmacol. 195, 370 378.
140. Kim, D. J., K. S. Prabhu, F. J. Gonzalez J. M. Peters (2006) Inhibition of chemically induced skin carcinogenesis by sulindac is independent of peroxisome proliferator-activated receptor-beta/delta (PPARbeta/delta). Carcinogenesis 27, 1105 1112.
141. Fischer, S. M., A. Pavone, C. Mikulec, R. Langenbach J. E. Rundhaug (2007) Cyclooxygenase-2 expression is critical for chronic UV-induced murine skin carcinogenesis. Mol. Carcinog. 46, 363 371.
142. Bol, D. K., R. B. Rowley, C. P. Ho, B. Pilz, J. Dell, M. Swerdel, K. Kiguchi, S. Muga, R. Klein S. M. Fischer (2002) Cyclooxygenase-2 overexpression in the skin of transgenic mice results in suppression of tumor development. Cancer Res. 62, 2516 2521.
143. Rundhaug, J. E., A. Pavone, E. Kim S. M. Fischer (2007) The effect of cyclooxygenase-2 overexpression on skin carcinogenesis is context dependent. Mol. Carcinog. 46, 981 992.
144. Groves, R. W., H. Mizutani, J. D. Kieffer T. S. Kupper (1995) Inflammatory skin disease in transgenic mice that express high levels of interleukin 1 alpha in basal epidermis. Proc. Natl Acad. Sci. USA 92, 11874 11878.
145. Murphy, J. E., R. E. Morales, J. Scott T. S. Kupper (2003) IL-1 alpha, innate immunity, and skin carcinogenesis: The effect of constitutive expression of IL-1 alpha in epidermis on chemical carcinogenesis. J. Immunol. 170, 5697 5703.
146. Moore, R. J., D. M. Owens, G. Stamp, C. Arnott, F. Burke, N. East, H. Holdsworth, L. Turner, B. Rollins, M. Pasparakis, G. Kollias F. Balkwill (1999) Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat. Med. 5, 828 831.
147. Suganuma, M., S. Okabe, M. W. Marino, A. Sakai, E. Sueoka H. Fujiki (1999) Essential role of tumor necrosis factor alpha (TNF-alpha) in tumor promotion as revealed by TNF-alpha-deficient mice. Cancer Res. 59, 4516 4518.
148. Arnott, C. H., K. A. Scott, R. J. Moore, S. C. Robinson, R. G. Thompson F. R. Balkwill (2004) Expression of both TNF-alpha receptor subtypes is essential for optimal skin tumour development. Oncogene 23, 1902 1910.
149. Scott, K. A., R. J. Moore, C. H. Arnott, N. East, R. G. Thompson, B. J. Scallon, D. J. Shealy F. R. Balkwill (2003) An anti-tumor necrosis factor-alpha antibody inhibits the development of experimental skin tumors. Mol. Cancer Ther. 2, 445 451.
150. Coussens, L. M., C. L. Tinkle, D. Hanahan Z. Werb (2000) MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103, 481 490.
151. Coussens, L. M., W. W. Raymond, G. Bergers, M. Laig-Webster, O. Behrendtsen, Z. Werb, G. H. Caughey D. Hanahan (1999) Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev. 13, 1382 1397.
152. Ahmad, N., A. C. Gilliam, S. K. Katiyar, T. G. O'Brien H. Mukhtar (2001) A definitive role of ornithine decarboxylase in photocarcinogenesis. Am. J. Pathol. 159, 885 892.